Spatial and seasonal variability of human and fish viruses in mussels inside and offshore of Ravenna's harbour (Adriatic Sea, Italy).
Adriatic Sea
harbour
hepatitis A virus
mussel
nervous necrosis virus
norovirus
viral contamination
Journal
Journal of applied microbiology
ISSN: 1365-2672
Titre abrégé: J Appl Microbiol
Pays: England
ID NLM: 9706280
Informations de publication
Date de publication:
Mar 2021
Mar 2021
Historique:
received:
15
05
2020
revised:
17
07
2020
accepted:
24
07
2020
pubmed:
4
8
2020
medline:
7
5
2021
entrez:
4
8
2020
Statut:
ppublish
Résumé
This study aims to investigate the presence and spatial-seasonal variability of human and fish viruses in coastal marine systems using Ravenna's harbour area (Adriatic Sea, Italy) as a model. Human viruses (noroviruses and hepatitis A virus) and one of the most threatening finfish pathogens, the nervous necrosis virus (NNV), were investigated in mussels living inside and offshore Ravenna's harbour. Thirty-three and 36·7% of tested mussel samples resulted contaminated by human and fish viruses respectively. A different spatial-seasonal distribution was observed. Human viruses were detected mainly in inner port sites during colder months, while NNV was detected in both inside and offshore of Ravenna's harbour, mainly during warmer months. The presence of human viruses in the inner port close to the city centre could be attributed to wastewaters carrying pathogens in the port environment and this arises public health concerns, however, the presence of these viruses limited to the canal port during the winter can greatly reduce the risk to human health. Regarding NNV, the accumulation and release of viable virus by mussels, could represent a viral source for susceptible finfish. These findings reflect the different epidemiological features of these infections and indicate the importance to choose the correct indicator to monitor viral contaminations. The high frequency of viral contamination pointed out in the study stresses the imperative to monitor the viral presence in all coastal habitats where the high natural value meets several recreational and commercial activities such as the Ravenna's harbour area. Particularly, this study could represent a novel starting point for the development of a more structured bio-monitoring program, in order to ensure improved environmental management and safety of coastal areas.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
994-1008Informations de copyright
© 2020 The Society for Applied Microbiology.
Références
Abbiati, M., Mistri, M., Bartoli, M., Ceccherelli, V.U., Colangelo, M.A., Ferrari, C.R., Giordani, G., Munari, C. et al. (2010) Trade-off between conservation and exploitation of the transitional water ecosystems of the northern Adriatic Sea. Chem Ecol 26, 105-119.
Airoldi, L. and Beck, M.W. (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol Annu Rev 45, 345-405.
Airoldi, L., Ponti, M. and Abbiati, M. (2016) Conservation challenges in human dominated seascapes: the harbour and coast of Ravenna. Reg Stud Mar Sci 8, 308-318.
Airoldi, L., Turon, X., Perkol-Finkel, S. and Rius, M. (2015) Corridors for aliens but not for natives: effects of marine urban sprawl at a regional scale. Divers Distrib 21, 755-768.
Boxman, I.L., Tilburg, J.J., Te Loeke, N.A., Vennema, H., Jonker, K., Deboer, E. and Koopmans, M. (2006) Detection of noroviruses in shellfish in the Netherlands. J Food Microbiol 108, 391-396.
Burkhardt, W. III, Watkins, W.D. and Rippey, S.R. (1992) Seasonal effects on accumulation of microbial indicator organisms by Mercenaria mercenaria. Appl Environ Microbiol 58, 826-831.
Chironna, M., Grottola, A., Lanave, C., Villa, E., Barbuti, S. and Quarto, M. (2003) Genetic analysis of HAV strains recovered from patients with acute hepatitis from southern Italy. J Med Virol 70, 343-349.
Ciulli, S., Gallardi, D., Scagliarini, A., Battilani, M., Hedrick, R.P. and Prosperi, S. (2006) Temperature-dependency of Betanodavirus infection in SSN-1 cell line. Dis Aquat Organ 68, 261-265.
Ciulli, S., Galletti, E., Grodzki, M., Alessi, A., Battilani, M. and Prosperi, S. (2007) Isolation and genetic characterization of Betanodavirus from wild marine fish from the Adriatic Sea. Vet Res Commun 31, 221-224.
Ciulli, S., Grodzki, M., Bignami, G., Serratore, P. and Prosperi, S. (2010) Molecular detection and genetic analysis of Betanodavirus in bivalve mollusk. J Biotechnol 150S, S4.
Ciulli, S., Volpe, E., Pagliarani, A., Zavatta, E., Brunetti, B., Gazzotti, T., Parmeggiani, A., Govoni, N.et al. (2017) A preliminary study on a novel sea water disinfection process by a peroxy-acid compound to complement and improve the microbial depuration of clams (Ruditapes philippinarum). Food Control 80, 226-235.
Croci, L., Losio, M.N., Suffredini, E., Pavoni, E. and Di Pasquale, S. (2007) Assessment of human enteric viruses in shellfish from the northern Adriatic Sea. Int J Food Microbiol 114, 252-257.
Da Silva, A.K., Le Saux, J.C., Parnaudeau, S., Pommepuy, M., Elimelech, M. and Le Guyader, F.S. (2007) Evaluation of removal of noroviruses during wastewater treatment using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Appl Environ Microbiol 73, 7891-7897.
Doan, Q.K., Vandeputte, M., Chatain, B., Morin, T. and Allal, F. (2017) Viral encephalopathy and retinopathy in aquaculture: a review. J Fish Dis 40, 717-742.
Drake, L., Doblin, M.A. and Dobbs, F.C. (2007) Potential microbial bioinvasions via ships’ ballast water, sediment, and biofilm. Mar Pollut Bull 55, 333-341.
Fabi, G., Grati, F., Puletti, M. and Scarcella, G. (2004) Effects on fish community induced by installation of two gas platforms in the Adriatic Sea. Mar Ecol Progr Ser 273, 187-197.
Goldbergh, E.D., Bowen, V.T., Farrington, J.W., Harvey, G., Martin, J.H., Parker, P.L., Risebrough, R.W., Robertson, W.et al. (1978) The mussel watch. Environ Conserv 5, 101-125.
Gonçalves, J., Gutiérrez-Aguirre, I., Balasubramanian, M.N., Zagorščak, M., Ravnikar, M. and Turk, V. (2018) Surveillance of human enteric viruses in coastal waters using concentration with methacrylate monolithic supports prior to detection by RT-qPCR. Mar Pollut Bull 128, 307-317.
Green, J., Henshilwood, K., Gallimore, C.I., Brown, D.W. and Lees, D.N. (1998) A nested reverse transcriptase PCR assay for detection of small round-structured viruses in environmentally contaminated molluscan shellfish. Appl Environ Microbiol 64, 858-863.
Henigman, U., Biasizzo, M., Vadnjal, S., Toplak, I., Gombac, M., Steyer, A., Prijatelj, M.P., Ambrozic, M. et al. (2015) Molecular characterization of noroviruses detected in mussels (Mytilus galloprovincialis) from harvesting areas in Slovenia. New Microbiol 38, 225-233.
Ilic, N., Velebit, B., Teodorovic, V., Djordjevic, V., Karabasil, N., Vasilev, D., Djuric, S., Adzic, B.et al. (2017) Influence of environmental conditions on norovirus presence in mussels harvested in Montenegro. Food Environ Virol 9, 406-414.
Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F.b, Takeda, N. and Katayama, K. (2003) Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41, 1548-1557.
Kim, Y., Aw, T.G. and Rose, J.B. (2016) Transporting oceanic viromes: Invasion of the aquatic biosphere. PLoS One 11, e0152671.
Kim, Y.C., Kwon, W.J., Kim, M.S., Kim, K.I., Min, J.G. and Jeong, H.D. (2018) High prevalence of betanodavirus barfin flounder nervous necrosis virus as well as red-spotted grouper nervous necrosis virus genotype in shellfish. J Fish Dis 41, 233-246.
Kroneman, A., Vennema, H., Deforche, K., Avoort, H.V., Peňarada, S., Oberste, M.S., Vinjé, J. and Koopmans, M. (2011) An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51, 121-125.
La Bella, G., Martella, V., Basanisi, M.G., Nobili, G., Terio, V. and La Salandra, G. (2017) Food-borne viruses in shellfish: Investigation on norovirus and HAV presence in Apulia (SE Italy). Food Environ Virol 9, 179-186.
Le Guyader, F., Dubois, E., Menard, D. and Pommepuy, M. (1994) Detection of hepatitis A virus, rotavirus, and enterovirus in naturally contaminated shellfish and sediment by reverse transcription-seminested PCR. Appl Environ Microbiol 60, 3665-3671.
Lipp, E.K., Kurz, R., Vincent, R. and Rodriguez-Palacios, C. (2001) The effects of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary. Estuaries 24, 266-276.
Loisy, F., Atmar, R.L., Gullon, P., Le Cann, P., Pommepuy, M. and Le Guyader, F.S. (2005) Real-time RT-PCR for norovirus screening in shellfish. J Virol Methods 123, 1-7.
Maalouf, H., Pommepuy, M. and Le Guyader, F.S. (2010) Environmental conditions leading to shellfish contamination and related outbreaks. Food Environ Virol 2, 136-145.
Markich, S.J. and Jeffree, R.A. (2019) The euryhaline pygmy mussel, Xenostrobus securis, is a useful biomonitor of key metal contamination in the highly urbanised Sydney Estuary, Australia. Environ Pollut 252, 813-824.
Mbayed, V.A., Sookoian, S., Alfonso, V. and Campos, R.H. (2002) Genetic characterization of hepatitis A virus isolates from Buenos Aires, Argentina. J Med Virol 68, 168-174.
Medici, M.C., Tummolo, F., Martella, V., Chezzi, C., Arcangeletti, M.C., De conto, F. and Calderaro, A. (2014) Epidemiological and molecular features of norovirus infections in Italian children affected with acute gastroenteritis. Epidemiol Infect 142, 2326-2335.
Middleboe, M. and Brussaard, C.P.D. (2017) Marine viruses: key players in marine ecosystems. Viruses 9, 302.
Molloy, S.D., Pietrak, M.R., Bricknell, I. and Bouchard, D.A. (2013) Experimental transmission of infectious pancreatic necrosis virus from the blue mussel, Mytilus edulis, to cohabitating Atlantic salmon (Salmo salar) smolts. Appl Env Microbiol 79, 5882-5890.
Munn, C. (2006) Viruses as pathogens of marine organisms- from bacteria to whales. J Mar Biol Ass UK 86, 453-467.
Nishizawa, T., Mori, K., Nakai, T., Furusawa, I. and Muroga, K. (1994) Polymerase chain reaction (PCR) amplification of RNA of striped jack nervous necrosis virus (SJNNV). Dis Aquat Organ 18, 103-107.
Occhipinti-Ambrogi, A. (2000) Biotic invasions in a Mediterranean Lagoon. Biol Invasions 2, 165-176.
Olveira, J.G., Souto, S., Dopazo, C.P., Thiéry, R., Barja, J.L. and Bandín, I. (2009) Comparative analysis of both genomic segments of betanodaviruses isolated from epizootic outbreaks in farmed fish species provides evidence for genetic reassortment. J Gen Virol 90, 2940-2951.
Panzarin, V., Fusaro, A., Monne, I., Cappellozza, E., Patarnello, P., Bovo, G., Capua, I., Holmes, E.C. et al. (2012) Molecular epidemiology and evolutionary dynamics of betanodavirus in southern Europe. Infect Genet Evol 12, 53-61.
Ponti, M., Abbiati, M. and Ceccherelli, V.U. (2002) Drilling platforms as artificial reefs: distribution of microbenthic assemblages of the “Paguro” wreck (northern Adriatic Sea). ICES J Mar Sci 59, S316-S323.
Ponti, M., Colangelo, M.A. and Ceccherelli, V.U. (2007) Composition, biomass and secondary production of the macrobenthic invertebrate assemblages in a coastal lagoon exploited for extensive aquaculture: Valle Smarlacca (northern Adriatic Sea). Estuar Coast Shelf S 75, 79-89.
Ponti, M., Pasteris, A., Guerra, R. and Abbiati, M. (2009) Impacts of maintenance channel dredging in a northern Adriatic coastal lagoon. II: Effects on macrobenthic assemblages in channels and ponds. Estuar Coast Shelf Sci 85, 143-150.
Ponti, M., Casselli, C. and Abbiati, M. (2011) Anthropogenic disturbance and spatial heterogeneity of macrobenthic invertebrate assemblages in coastal lagoons: the study case of Pialassa Baiona (northern Adriatic Sea). Helgol Mar Res 65, 25-42.
Ponti, M., Castellini, A., Ragazzoni, A., Gamba, E., Ceccherelli, V.U. and Abbiati, M. (2017) Decline of the Manila clams stock in the northern Adriatic lagoons: a survey on ecological and socio-economic aspects. Acta Adriat 58, 89-104.
Pranovi, F., Colla, S., Valeri, P. and Anelli Monti, M. (2016) Present and future status of artisanal fisheries in the Adriatic Sea (western Mediterranean Sea). Ocean Coast Manage 122, 49-56.
Serratore, P., Ciulli, S., Piano, A. and Cariani, A. (2014) Criticism of the purification process of bivalve shellfish: literature review and our industrial research experiences. In Shellfish Human Consumption, Health Implications and Conservation Concerns ed. Hay, R.M. pp. 1-50. New York, NY: Nova Science Publishers Inc.
Svraka, S., Duizer, E., Vennema, H., de Bruin, E., van der Veer, B., Dorresteijn, B. and Koopmans, M. (2007) Etiological role of viruses in outbreaks of acute gastroenteritis in the Netherlands from 1994 through 2005. J Clin Microbiol 45, 1389-1394.
Suffredini, E., Corrain, C., Arcangeli, G., Fasolato, L., Manfrin, A., Rossetti, E., Biazzi, E., Mioni, R. et al. (2008) Occurrence of enteric viruses in shellfish and relation to climatic-environmental factors. Lett Appl Microbiol 47, 467-474.
Suffredini, E., Magnabosco, C., Civettini, M., Rossetti, E., Arcangeli, G. and Croci, L. (2012) Norovirus contamination in different shellfish species harvested in the same production areas. J Appl Microbiol 113, 686-692.
Toffolo, V., Negrisolo, E., Maltese, C., Bovo, G., Belvedere, P., Colombo, L. and Valle, L.D. (2007) Phylogeny of betanodaviruses and molecular evolution of their RNA polymerase and coat proteins. Mol Phylogenet Evol 43, 298-308.
van Beek, J., de Graaf, M., Al-Hello, H., Allen, D.J., Ambert-Balay, K., Botteldoorn, N., Brytting, M., Buesa, J.et al. (2018) Molecular surveillance of norovirus, 2005-16: an epidemiological analysis of data collected from the NoroNet network. The Lancet Infect Dis 18, 545-553.
Vendramin, N., Patarnello, P., Toffan, A., Panzarin, V., Cappellozza, E., Tedesco, P., Terlizzi, A. and Terregino, C. et al. (2013) Viral encephalopathy and retinopathy in groupers (Epinephelus spp.) in southern Italy: a threat for wild endangered species. BMC Vet Res 9, 20.
Verhoef, L., Hewitt, J., Barclay, L., Ahmed, S.M., Lake, B., Hall, A.J., Lopman, B., Kroneman, A.et al. (2015) Norovirus genotype profiles associated with foodborne transmission, 1999-2012. Emerg Infect Dis 21, 592-599.
Vinjé, J. and Koopmans, M.P.G. (1996) Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J Infect Dis 174, 610-615.
Volpe, E., Pagnini, N., Serratore, P. and Ciulli, S. (2017) Fate of redspottet grouper nervous necrosis virus (RGNNV) in experimentally challenged Manila clam Ruditapes philippinarum. Dis Aquat Organ 125, 53-61.
Volpe, E., Grodzki, M., Panzarin, V., Guercio, A., Purpari, G., Serratore, P. and Ciulli, S. (2018) Detection and molecular characterization of betanodaviruses retrieved from bivalve molluscs. J Fish Dis 41, 603-611.
Volpe, E., Gustinelli, A., Caffara, M., Errani, F., Quaglio, F., Fioravanti, M.l. and Ciulli, S. (2020) Viral nervous necrosis outbreaks caused by the RGNNV/SJNNV reassortant betanodavirus in gilthead sea bream (Sparus aurata) and European sea bass (Dicentrarchus labrax). Aquaculture 523, 735155. https://doi.org/10.1016/j.aquaculture.2020.735155.
Wang, Y., Zhang, J. and Shen, Z. (2015) The impact of calicivirus mixed infection in an oyster-associated outbreak during a food festival. J Clin Virol 73, 55-63.
Wyn-Jones, P.A., Carducci, A., Cook, N., D’Agostino, M., Divizia, M., Fleischer, J., Gantzer, C., Gawler, A.et al. (2011) Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res 45, 1025-1038.